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North Andean origin and diversification of the largest ithomiine butterfly genus

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ABSTRACT

The Neotropics harbour the most diverse flora and fauna on Earth. The Andes are a major centre of diversification and source of diversity for adjacent areas in plants and vertebrates, but studies on insects remain scarce, even though they constitute the largest fraction of terrestrial biodiversity. Here, we combine molecular and morphological characters to generate a dated phylogeny of the butterfly genus Pteronymia (Nymphalidae: Danainae), which we use to infer spatial, elevational and temporal diversification patterns. We first propose six taxonomic changes that raise the generic species total to 53, making Pteronymia the most diverse genus of the tribe Ithomiini. Our biogeographic reconstruction shows that Pteronymia originated in the Northern Andes, where it diversified extensively. Some lineages colonized lowlands and adjacent montane areas, but diversification in those areas remained scarce. The recent colonization of lowland areas was reflected by an increase in the rate of evolution of species’ elevational ranges towards present. By contrast, speciation rate decelerated with time, with no extinction. The geological history of the Andes and adjacent regions have likely contributed to Pteronymia diversification by providing compartmentalized habitats and an array of biotic and abiotic conditions, and by limiting dispersal between some areas while promoting interchange across others.

No MeSH data available.


BEAST dated species-level phylogeny of the genus Pteronymia and outgroups, based on molecular and morphological characters.Main clades and secondary calibration points based on butterfly (red circles) and host-plant ages (green circles) are indicated and corresponding age priors are shown in the table inserted in the figure. The figure was generated with FigTree (http://tree.bio.ed.ac.uk/software/figtree/) and edited with Adobe Illustrator 4 (http://www.adobe.com/uk/products/illustrator.html). Butterfly pictures were taken by Keith Willmott and edited in Adobe Photoshop CS4 (www.adobe.com/products/photoshop/) and correspond to butterfly names in red in adjacent phylogeny.
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f1: BEAST dated species-level phylogeny of the genus Pteronymia and outgroups, based on molecular and morphological characters.Main clades and secondary calibration points based on butterfly (red circles) and host-plant ages (green circles) are indicated and corresponding age priors are shown in the table inserted in the figure. The figure was generated with FigTree (http://tree.bio.ed.ac.uk/software/figtree/) and edited with Adobe Illustrator 4 (http://www.adobe.com/uk/products/illustrator.html). Butterfly pictures were taken by Keith Willmott and edited in Adobe Photoshop CS4 (www.adobe.com/products/photoshop/) and correspond to butterfly names in red in adjacent phylogeny.

Mentions: We combined morphological and molecular data to generate a species-level phylogeny that was calibrated using secondary calibrations from a published Nymphalidae phylogeny39, and from Solanaceae lineage ages estimated in this study, using BEAST 1.7.545. This resulted in 901 trees (after burnin), from which we extracted the maximum clade credibility tree with median branch length (hereafter MCC tree). The combination of morphological and molecular data generated a phylogeny comprising all known extant species (Fig. 1). Many nodes were poorly supported, and this was mostly caused by the species represented only by morphological characters, whose placement was uncertain. Our calibration strategy that combined butterfly- and host-plant-derived secondary calibrations resulted in ages that were about 30 to 50% older than those inferred in a recent time-calibrated phylogeny of Ithomiini genera that relied on previous minimum age estimate of Solanaceae lineages38. By contrast, our ages were often slightly younger, but well within the credibility interval of the ages estimated in the Nymphalidae phylogeny39. Notably, the stem age of Pteronymia inferred in our study is 14.4 million years (my) [12.3–16.3], while it was 7.5 my [6.0–9.0] in the higher level Ithomiini phylogeny38 and 15.7 my [11.5–18.5] in the Nymphalidae phylogeny39. We repeated this analysis without the Solanaceae calibrations and this had little impact on most nodes of the phylogeny. The greatest difference was found for the divergence between the outgroup genera Athesis and Patricia (22.9 million years ago (mya) [20.0–24.0] under the combined calibration scheme, 25.4 mya [21.8–27.5] with Nymphalidae calibrations only). For the genus Pteronymia, ages under the two calibration schemes were extremely similar (regression ages Nymphalidae calibration only (N) versus combined Nymphalidae and Solanaceae (S): N = 0.989*S, r2 = 0.997). Trees generated under the combined calibration scheme were used in all subsequent analyses.


North Andean origin and diversification of the largest ithomiine butterfly genus
BEAST dated species-level phylogeny of the genus Pteronymia and outgroups, based on molecular and morphological characters.Main clades and secondary calibration points based on butterfly (red circles) and host-plant ages (green circles) are indicated and corresponding age priors are shown in the table inserted in the figure. The figure was generated with FigTree (http://tree.bio.ed.ac.uk/software/figtree/) and edited with Adobe Illustrator 4 (http://www.adobe.com/uk/products/illustrator.html). Butterfly pictures were taken by Keith Willmott and edited in Adobe Photoshop CS4 (www.adobe.com/products/photoshop/) and correspond to butterfly names in red in adjacent phylogeny.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC5384087&req=5

f1: BEAST dated species-level phylogeny of the genus Pteronymia and outgroups, based on molecular and morphological characters.Main clades and secondary calibration points based on butterfly (red circles) and host-plant ages (green circles) are indicated and corresponding age priors are shown in the table inserted in the figure. The figure was generated with FigTree (http://tree.bio.ed.ac.uk/software/figtree/) and edited with Adobe Illustrator 4 (http://www.adobe.com/uk/products/illustrator.html). Butterfly pictures were taken by Keith Willmott and edited in Adobe Photoshop CS4 (www.adobe.com/products/photoshop/) and correspond to butterfly names in red in adjacent phylogeny.
Mentions: We combined morphological and molecular data to generate a species-level phylogeny that was calibrated using secondary calibrations from a published Nymphalidae phylogeny39, and from Solanaceae lineage ages estimated in this study, using BEAST 1.7.545. This resulted in 901 trees (after burnin), from which we extracted the maximum clade credibility tree with median branch length (hereafter MCC tree). The combination of morphological and molecular data generated a phylogeny comprising all known extant species (Fig. 1). Many nodes were poorly supported, and this was mostly caused by the species represented only by morphological characters, whose placement was uncertain. Our calibration strategy that combined butterfly- and host-plant-derived secondary calibrations resulted in ages that were about 30 to 50% older than those inferred in a recent time-calibrated phylogeny of Ithomiini genera that relied on previous minimum age estimate of Solanaceae lineages38. By contrast, our ages were often slightly younger, but well within the credibility interval of the ages estimated in the Nymphalidae phylogeny39. Notably, the stem age of Pteronymia inferred in our study is 14.4 million years (my) [12.3–16.3], while it was 7.5 my [6.0–9.0] in the higher level Ithomiini phylogeny38 and 15.7 my [11.5–18.5] in the Nymphalidae phylogeny39. We repeated this analysis without the Solanaceae calibrations and this had little impact on most nodes of the phylogeny. The greatest difference was found for the divergence between the outgroup genera Athesis and Patricia (22.9 million years ago (mya) [20.0–24.0] under the combined calibration scheme, 25.4 mya [21.8–27.5] with Nymphalidae calibrations only). For the genus Pteronymia, ages under the two calibration schemes were extremely similar (regression ages Nymphalidae calibration only (N) versus combined Nymphalidae and Solanaceae (S): N = 0.989*S, r2 = 0.997). Trees generated under the combined calibration scheme were used in all subsequent analyses.

View Article: PubMed Central - PubMed

ABSTRACT

The Neotropics harbour the most diverse flora and fauna on Earth. The Andes are a major centre of diversification and source of diversity for adjacent areas in plants and vertebrates, but studies on insects remain scarce, even though they constitute the largest fraction of terrestrial biodiversity. Here, we combine molecular and morphological characters to generate a dated phylogeny of the butterfly genus Pteronymia (Nymphalidae: Danainae), which we use to infer spatial, elevational and temporal diversification patterns. We first propose six taxonomic changes that raise the generic species total to 53, making Pteronymia the most diverse genus of the tribe Ithomiini. Our biogeographic reconstruction shows that Pteronymia originated in the Northern Andes, where it diversified extensively. Some lineages colonized lowlands and adjacent montane areas, but diversification in those areas remained scarce. The recent colonization of lowland areas was reflected by an increase in the rate of evolution of species’ elevational ranges towards present. By contrast, speciation rate decelerated with time, with no extinction. The geological history of the Andes and adjacent regions have likely contributed to Pteronymia diversification by providing compartmentalized habitats and an array of biotic and abiotic conditions, and by limiting dispersal between some areas while promoting interchange across others.

No MeSH data available.